Leontopithecus rosalia, Golden Lion Tamarinbichodomatoip.org/wp-content/uploads/2020/03/Ruiz...Golden lion tamarins are an adaptable species well able to live in degraded and secondary

The IUCN Red List of Threatened Species™ISSN 2307-8235 (online)IUCN 2019: T11506A17935211Scope: GlobalLanguage: English

Leontopithecus rosalia, Golden Lion Tamarin

Assessment by: Ruiz-Miranda, C.R., Jerusalinsky, L., Kierulff, C., Mittermeier,R.A., Oliveira, L., Pissinatti, A., Valença Montenegro, M. & de Oliveira, P.

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Citation: Ruiz-Miranda, C.R., Jerusalinsky, L., Kierulff, C., Mittermeier, R.A., Oliveira, L., Pissinatti, A.,Valença Montenegro, M. & de Oliveira, P. 2019. Leontopithecus rosalia. The IUCN Red List ofThreatened Species 2019: e.T11506A17935211. http://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T11506A17935211.en

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Taxonomy

Kingdom Phylum Class Order Family

Animalia Chordata Mammalia Primates Callitrichidae

Taxon Name: Leontopithecus rosalia (Linnaeus, 1766)

Common Name(s):

• English: Golden Lion Tamarin• French: Singe-lion, Tamarin Soyeux

Taxonomic Notes:

The lion tamarins, Leontopithecus, are listed as separate species following Della Serra (1951),Rosenberger and Coimbra-Filho (1984), Mittermeier et al. (1988), Natori (1989), and Rylands et al.(1993). They have been listed as subspecies of L. rosalia by Coimbra-Filho and Mittermeier (1972, 1973),Hershkovitz (1977), Mittermeier and Coimbra-Filho (1981), Forman et al. (1986) and Seuánez et al.(1988), the latter two publications on the basis of identical chromosome morphologies.

Assessment Information

Red List Category & Criteria: Endangered A3cde ver 3.1

Year Published: 2019

Date Assessed: January 26, 2015

Justification:

Leontopithecus rosalia is considered Endangered under criteria EN A3ce, an anticipated populationreduction of 50% over the course of the next three generations (2019-2039) due to a loss of habitatquality (i.e., impacts of urbanization and fragmentation due to an expanding road network), resourcecompetition with introduced Callithrix jacchus, hybridization with introduced L. chrysomelas, and thethe negative impacts of stochastic events (e.g., recent yellow fever outbreak).

Previously Published Red List Assessments

2008 – Endangered (EN)http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T11506A3287321.en

2003 – Endangered (EN)

2000 – Critically Endangered (CR)

1996 – Critically Endangered (CR)

1994 – Endangered (E)




© The IUCN Red List of Threatened Species: Leontopithecus rosalia – published in 2019.http://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T11506A17935211.en

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Geographic Range

Range Description:

The centre of the range of L. rosalia is the basin of the Rio São João, state of Rio de Janeiro. The originaldistribution was first clarified by Coimbra-Filho (1969, 1976) and Coimbra-Filho and Mittermeier (1973,1977). It covered the majority of the lowland coastal region of the state of Rio de Janeiro, up to 300 masl. The easternmost record for the species is Mangaratiba, on the coast in the south-east of the state.The original distribution included all or parts of the following municipalities: Mangaratiba, Itaguai, NovaIguaçú, Nilópolis, São João do Meriti, Duque de Caxias, Rio de Janeiro, Magé, São Gonçalo, Niterói,Itaborai, Maricá, Araruama, Silva Jardim, Saquarema, Rio Bonito, Cachoeiras de Macucu, São Pedro daAldeia, Cabo Frio, Casimiro de Abreu, Macaé, Conceição de Macabu, Campos, and São João da Barra.

From his surveys carried out between 1962 and 1969, Coimbra-Filho concluded that L. rosalia wasextinct in all but seven (Silva Jardim, Cabo Frio, Saquarema, Aruarama, Casimiro de Abreu, Rio Bonito,and São Pedro da Aldeia) of the 24 municipalities of its original range. The exhaustive survey by Kierulff(1993a,b; Kierulff and Procópio de Oliveira 1996; Kierulff and Rylands 2003) which covered the entirerange of the species during 18 months between 1990 and 1992, showed that they remain in only 104.5km² of forests in three regions: 1) near the coast (the Centro Hípico de Cabo Frio, with an estimated 29individuals, and Campos Novos, with an estimated 36 individuals); 2) the Poço das Antas BiologicalReserve and adjacent forests (with an estimated 360 individuals); and 3) on the hillsides of the Serra doMar (with an estimated 74 individuals), there largely restricted to lowland forest patches. A further ninelocalities contained 12 isolated groups, totalling 60 individuals. These subpopulations were registered injust four of the municipalities reported by Coimbra-Filho (1969): Silva Jardim, Cabo Frio, Saquarema, andAruarama, the latter two, however, maintaining only a single group each (Kierulff 1993a).

Burity et al. (2007) reported the occurrence of L. rosalia in the municipality of Duque de Caxias, near theRio Taquara, in the Taquara Municipal Natural Park (19,000 ha), Rio de Janeiro, a westward extension ofits current known range.During 2014, the Golden Lion Tamarin Association, in collaboration withresearchers from the Universidade Estadual do Norte fluminense (M de Morais and CR Ruiz-Miranda)carried out an intensive survey on the São João River watershed (covers the Biological Reserves and theFederally Protected region were 90% of the population is presumed to be) using an improved playbacktechnique and a single-season occupancy model (MacKenzie et al. 2002). The results estimate a totalpopulation of 3400 tamarins and detected the presence of tamarins in several fragments were they hadnot previously been detected. The survey provided an accurate estimate of GLT occurrence over thewhole region, pointing out areas of low probability of occurrence or gaps in the distribution. In 2014,the AMLD team counted an additional 106 tamarins in the Cabo Frio Municipal Park. The extent ofoccurrence of L. rosalia was calculated using the MCP (Minimum Convex Polygon) taking into accountonly the occupied fragments, then excluding areas with local extinction (Pissinatti A., personalcommunication). Therefore, the calculated extent of occurrence was 6106.23 km2 and the estimatedarea of occupancy was less than 500 km2 (337.55 km2) (Traylor-Holzer 2006).

Country Occurrence:

Native: Brazil (Rio de Janeiro)


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Distribution MapLeontopithecus rosalia


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PopulationIn 2003, the species was downlisted from Critically Endangered to Endangered, as a result of nearlythirty years of conservation efforts, involving numerous institutions, through the Golden Lion TamarinConservation Program (GLTCP) of the National Zoological Park, Smithsonian Institution, Washington, DC,and the Associação Mico-Leao-Dourado, Rio de Janeiro. Conservation efforts have included theestablishment of a new population through translocation of 47 individuals in six groups, each isolatedand evidently otherwise doomed in tiny isolated forests elsewhere, to a new protected area, the UniãoBiological Reserve. Currently, about one-third of the wild population are descendants of a reintroductionprogramme. The reintroduction of captive-born Golden Lion Tamarins has contributed significantly notonly to the numbers living in the wild, but also to the protection of 3,100 ha of forests within their range(Beck et al. 1986, 1991, 1994; Stoinski et al. 1997; Beck and Martins 1999, 2001).

Early estimates of population size ranged from 200-600 (Coimbra-Filho 1969; Coimbra-Filho andMittermeier 1973, 1977), but it was only in 1991-1992 that a full and thorough census was carried outby Kierulff (1993a,b; Kierulff and Procópio de Oliveira 1996). Not including the population in the Poçodas Antas Biological Reserve, the total number of individuals estimated was 272 in 55 groups. They weredivided amongst 14 forests - four main subpopulations with six or more groups each and 12 groupsisolated in 10 forest fragments each of 200 ha or less in area. The total area of forest containing GoldenLion Tamarins was 104.5 km². The majority of groups (29) were located in the municipality of SilvaJardim (53%), 24 groups were located in Cabo Frio (43%), and one group each were found in themunicipalities of Saquarema and one in Araruama. At the time, the Poço das Antas Biological Reservewas known to harbour about 290 lion tamarins (Kierulff 1993a), giving a total population of 562 (range470-631), close to the estimate of Coimbra-Filho in 1969.

During Kierulff's (1993) census, the population of reintroduced lion tamarins was 118 individuals, but byDecember 2000, the number had risen to 359 (Kierulff et al. 2002a, b). A translocation programme,begun in 1994, established a new and thriving population in the União Biological Reserve, with sixintroduced groups resulting in a population of over 120 lion tamarins in the Reserve by mid-2001(Kierulff et al. 2002a). The forests targeted for re-introduction are now believed to be at carryingcapacity, and Kierulff and Procópio de Oliveira (1996) estimated that the União Biological Reserve (at2,400 ha the second largest single block of lowland forest in the state, after the marginally larger Poçodas Antas Biological Reserve, with 2,760 ha of forest) can hold no more than about 158 lion tamarins (33groups).

From 1997 to 2000 the numbers in the Poço das Antas Biological Reserve declined due to predation tojust 220 animals (see Franklin and Dietz 2001), but since the population has recovered to an estimated408 animals (AMLD, unpublished data).

Based on Kierulff's 1993 census, the population of reintroduced golden lion tamarins was 118. ByDecember 2000 the number had risen to 359 (Kierulff et al. 2002a,b). A translocation programme,begun in 1994, established a new and thriving population in the União Biological Reserve; six introducedgroups yielded a population of >120 lion tamarins by mid-2001 (Kierulff et al. 2002a). The foreststargeted for re-introduction are now believed to be at carrying capacity. Kierulff and Procópio deOliveira (1996) estimated that the 2,400-ha União Biological Reserve (the second largest single block oflowland forest in the state) can hold no more than about 158 lion tamarins (33 groups). The most


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recent population estimate for Leontopithecus rosalia, based on 3,200 individuals in the Sao Joao andMacae River Basins (AMLD 2018), would be just above 3,700 (Ruiz-Miranda et al. 2019). Based upon anaverage group size of five for the genus Leontopithecus, with two mature individuals per group, the totalnumber of mature individuals would be approximately 1,400. However, subsequent to data collectionfor the most recent population estimate, GLT populations were hit by yellow fever. Replicated surveys ineach of 13 forest fragments holding L. rosalia yield an overall population loss of 32% (J. Dietzunpublished data).

Current Population Trend: Decreasing

Habitat and Ecology (see Appendix for additional information)An inhabitant of lowland seasonal rainforest of the Atlantic coast of Brazil, with an average annualrainfall of around 1,500 mm a year (Rylands 1993). Golden lion tamarins are an adaptable species wellable to live in degraded and secondary forests, depending only on sufficient year round food sourcesand foraging sites, along with the tree holes they use as sleeping sites (see Coimbra-Filho 1969, 1976;Coimbra-Filho and Mittermeier 1973).

Marmosets and tamarins are distinguished from the other monkeys of the New World by their smallsize; modified claws rather than nails on all digits except the big toe; the presence of two as opposed tothree molar teeth in either side of each jaw, and by the occurrence of twin births. They eat fruits,flowers, nectar, plant exudates (gums) and animal prey (including frogs, snails, lizards, spiders andinsects).

A book edited by Kleiman and Rylands (2002) contains chapters that extensively review behaviouralecology, reproductive biology, mating systems, infant care, vocal communication, conservation statusand reintroduction biology. A more recent book edited by Oliveria et al. (2008) reviews information onhabitat fragmentation, invasive species and conservation strategies for golden lion tamarins. Liontamarins are an insectivore-frugivore species, with opportunistic consumption of tree exudates. Theydiffer from other callitrichids in having long fingers and hands, which allow them to forage for preyefficiently in nooks and crannies and in epiphytic tank bromeliads. Lion tamarins live in extended familygroups of usually 4 to 8 individuals. For L. rosalia, Dietz and Kleiman (1986) recorded a mean group sizeof 5.8 (range 3-11, n=21) at the Poço das Antas Biological Reserve. Recently, Hankerson and Dietz (2014)compared group sizes in two different predation periods. Average group size (excluding infants) was 4.4individuals during high predation periods and 6.0 individuals during low predation periods (Hankersonand Dietz 2014). Generally, only one female per group breeds during a particular breeding season. Theybreed once or twice a year. There is cooperative care of the young. Both sexes disperse. Averagedispersal distance is 847 meters (Mickleberg, 2011). The groups defend home ranges of 40 to more than100 ha. Hankerson & Dietz (2014) reported home ranges sizes based on different group sizes (small(8 individuals) in Poço das Antas BiologicalReserve. The authors found home ranges varying from (mean ± SE) 66.9 ± 3.71 ha for large groups (N=17), 49.7 ± 1.96 ha for medium-sized groups (N=66) and 46.7 ± 1.99 ha (N=62) for small size groups.Important determinants of home range size were predation and future reproductive needs. At the UniãoBiological Reserve, home ranges average 150 ±72 ha (range 65-229 ha) (Kierulff 2000).

Systems: Terrestrial


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Threats (see Appendix for additional information)Historically, Leontopithecus rosalia has been threatened by severe forest loss and fragmentation, as wellas live capture for the pet trade. Today, the most severe threats facing this species are the urbanizationof former forests and pastureland, an expanding road network (e.g., BR 101) that further fragmentsremaining forest blocks and conservation management units, the potential for stochastic events such asa recent yellow fever outbreak, competition with introduced Callithrix jacchus, and hybridization withintroduced Leontopithecus chrysomelas (Bicca-Marques et al. 2017, Ruiz-Miranda et al. 2019, J. Dietzunpublished data). An overall population estimated at 3,700 (1,400 mature individuals) is spread amongnearly 20 sub-populations; 60% of these inhabit patches of 1,000 ha or less, 96% of which are less than100 ha (Kierulff and Procópio de Oliveira 1996). Many of the sub-populations are believed to havereached carrying capacity and are potentially non-viable in the long-term due to the potential forinbreeding depression (Kierulff and Procópio de Oliveira 1996, Dietz et al. 2000). A documentedreduction of L. rosalia of greater than 50% in the Poco das Antas Biological Reserve in the 1990s givescause for concern regarding the potential for significant population fluctuations (Franklin and Dietz2001), including a decline of more than 30% recently documented due to an outbreak fo yellow fever (J.Dietz unpublished data).

Conservation Actions (see Appendix for additional information)Included on the Brazilian Official List of Species Threatened with Extinction (Lista Nacional Oficial deEspécies da Fauna Ameaçadas de ExtinçãoMMA, 2014), and likewise on the regional threatened specieslist of the state of Rio de Janeiro (Bergallo et al. 2000). It is listed on Appendix I of CITES.The conservation project for the golden lion tamarins has been considered successful (Kierulff et al.2012). The first conservation initiatives for Leontopithecus rosalia began with field surveys and initiationof a breeding programme for the species by Adelmar Coimbra-Fillho and Alceo Magnanani in the late1960s (Coimbra-Filho and Magananini 1972; Magnanini and Coimbra-Filho 1972; Coimbra-Filho1976a,b). Kleiman (1972) set up an international breeding programme and studbook for the captivepopulations in 1972, and initiated The Golden Lion Tamarin Conservation Program (GLTCP) of theNational Zoological Park, Smithsonian Institution, in 1983. The GLTCP, subsumed by the Brazilian NGO-the Golden Lion Tamarin Association (AMLD),-in 1993, remains active and includes field research,reintroduction, environmental education, and habitat restoration programmes. Today the conservationefforts are centred on the São João River Watershed which includes the Poço das Antas BiologicalReserve, created in 1972 (Magnanini 1978), the União Biological Reserve (created in 2008), and the Sãojoão river-golden lion tamarin Federal Environmental Protection Area (created in 2002).Golden Lion Tamarins occur in the Poço das Antas Biological Reserve (5,500 ha, of which 2,760 ha isforested), União Biological Reserve (3,260 ha, of which 2,400 ha is forested), Bacia do Rio São João /Mico-leão-dourado Environmental Protection Area (150,700 ha), Petropólis Environmental ProtectionArea (5900 ha) (Burity et al. 2007,) and Taquara Municipal Natural Park (19,000 ha) (Burity et al. 2007).The Golden Lion Tamarin Association, a Brazilian NGO, founded in 1993 has a strong and active strategicmanagement plan for the conservation of the species in its habitat. A recent strategic planning meeting(2015) identified the key strategies for long term conservation of the species, and has a plan for forming4 major viable populations connected as a meta-population. There is a managed population in captivitymaintained at about 490 animals. There is some room for expansion for the population, but consideringthe extreme fragmentation there will be the need for active reforestation to increase forest connectivity.Current and future conservation efforts are attacking this problem with reforestation and theestablishment of corridors. There are ongoing translocation efforts to seed a new population in the area


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of Lavras/Pirinueus.The small threat posed by the introduced GHLTs in Niteroi is being further reducedby the removal of these animals from the region through a collaborative project carried by the InstitutoPri-Matas, INEA (Rio de Janeiro State Environmental Institute) and ICMBio. The project has removedover 500 of these animals. Total removal is planned to end by 2016. There was an International Committee for the Conservation and Management of Lion Tamarins, set upin 1990 by the Brazilian Government (Instituto do Meio Ambiente e dos Recursos Naturais Renováveisof the Ministry of the Environment) (see Rambaldi et al. 2002). It stopped working in 2005,approximately. The Instituto Chico Mendes de Conservação da Biodiversidade (of the Ministry of theEnvironment) incorporated the functions of that committee within is National Action Plan for theMammals of Central Atlantic Forest. Historical reviews of the conservation measures and programmes for the lion tamarins are provided byRylands et al. (2002), Rambaldi et al. (2002), Kierulff et al. (2002b), Beck et al. (2002), Valladares-Paduaet al. (2002), Padua et al. (2002), and Kleiman and Rylands (2002a).

Credits

Assessor(s): Ruiz-Miranda, C.R., Jerusalinsky, L., Kierulff, C., Mittermeier, R.A., Oliveira, L.,Pissinatti, A., Valença Montenegro, M. & de Oliveira, P.

Reviewer(s): Cotton, A., Molur, S. & Schwitzer, C.

Facilitators(s) andCompiler(s):

Angelico, M. & Konstant, W.R.


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management for the conservation of black lion tamarins. In: D. G. Kleiman and A. B. Rylands (eds), TheLion Tamarins of Brazil, pp. 301-314. Smithsonian Institution Press, Washington, DC, USA.

CitationRuiz-Miranda, C.R., Jerusalinsky, L., Kierulff, C., Mittermeier, R.A., Oliveira, L., Pissinatti, A., ValençaMontenegro, M. & de Oliveira, P. 2019. Leontopithecus rosalia. The IUCN Red List of Threatened Species2019: e.T11506A17935211. http://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T11506A17935211.en

DisclaimerTo make use of this information, please check the Terms of Use.

External ResourcesFor Images and External Links to Additional Information, please see the Red List website.


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Appendix

Habitats(http://www.iucnredlist.org/technical-documents/classification-schemes)

Habitat Season Suitability MajorImportance?

1. Forest -> 1.6. Forest - Subtropical/Tropical Moist Lowland - Suitable Yes

Threats(http://www.iucnredlist.org/technical-documents/classification-schemes)

Threat Timing Scope Severity Impact Score

1. Residential & commercial development -> 1.1.Housing & urban areas

Ongoing - - -

Stresses: 1. Ecosystem stresses -> 1.1. Ecosystem conversion

1. Ecosystem stresses -> 1.2. Ecosystem degradation

2. Agriculture & aquaculture -> 2.1. Annual &perennial non-timber crops -> 2.1.2. Small-holderfarming

Ongoing - - -



2. Agriculture & aquaculture -> 2.1. Annual &perennial non-timber crops -> 2.1.3. Agro-industryfarming

Ongoing - - -



2. Agriculture & aquaculture -> 2.2. Wood & pulpplantations -> 2.2.2. Agro-industry plantations

Future - - -



2. Agriculture & aquaculture -> 2.3. Livestock farming& ranching -> 2.3.3. Agro-industry grazing, ranchingor farming

Ongoing - - -



4. Transportation & service corridors -> 4.1. Roads &railroads

Ongoing - - -



7. Natural system modifications -> 7.1. Fire & firesuppression -> 7.1.3. Trend Unknown/Unrecorded

Ongoing - - -

Stresses: 1. Ecosystem stresses -> 1.2. Ecosystem degradation

Conservation Actions in Place(http://www.iucnredlist.org/technical-documents/classification-schemes)


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http://www.iucnredlist.org/technical-documents/classification-schemeshttp://www.iucnredlist.org/technical-documents/classification-schemeshttp://www.iucnredlist.org/technical-documents/classification-schemes

Conservation Actions in Place

In-Place Land/Water Protection and Management

Occur in at least one PA: Yes

In-Place Species Management

Successfully reintroduced or introduced beningly: Yes

Subject to ex-situ conservation: Yes

In-Place Education

Subject to recent education and awareness programmes: Yes

Included in international legislation: Yes

Subject to any international management/trade controls: Yes

Conservation Actions Needed(http://www.iucnredlist.org/technical-documents/classification-schemes)

Conservation Actions Needed

2. Land/water management -> 2.1. Site/area management

2. Land/water management -> 2.3. Habitat & natural process restoration

Research Needed(http://www.iucnredlist.org/technical-documents/classification-schemes)

Research Needed

1. Research -> 1.1. Taxonomy

1. Research -> 1.2. Population size, distribution & trends

1. Research -> 1.3. Life history & ecology

1. Research -> 1.5. Threats

1. Research -> 1.6. Actions

3. Monitoring -> 3.1. Population trends

Additional Data Fields

Distribution

Estimated area of occupancy (AOO) (km²): 337.55

Continuing decline in area of occupancy (AOO): Yes

Estimated extent of occurrence (EOO) (km²): 6106.23


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http://www.iucnredlist.org/technical-documents/classification-schemeshttp://www.iucnredlist.org/technical-documents/classification-schemes

Distribution

Lower elevation limit (m): 0

Upper elevation limit (m): 800

Population

Number of mature individuals: 1400

Continuing decline of mature individuals: Yes

No. of subpopulations: 18

Continuing decline in subpopulations: No

Extreme fluctuations in subpopulations: No

All individuals in one subpopulation: No

Habitats and Ecology

Continuing decline in area, extent and/or quality of habitat: Yes

Generation Length (years): 7


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The IUCN Red List of Threatened Species™ISSN 2307-8235 (online)IUCN 2019: T11506A17935211Scope: GlobalLanguage: English

The IUCN Red List Partnership

The IUCN Red List of Threatened Species™ is produced and managed by the IUCN Global SpeciesProgramme, the IUCN Species Survival Commission (SSC) and The IUCN Red List Partnership.

The IUCN Red List Partners are: Arizona State University; BirdLife International; Botanic GardensConservation International; Conservation International; NatureServe; Royal Botanic Gardens, Kew;Sapienza University of Rome; Texas A&M University; and Zoological Society of London.

THE IUCN RED LIST OF THREATENED SPECIES™


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Documents

Leontopithecus rosalia, Golden Lion Tamarinbichodomatoip.org/wp-content/uploads/2020/03/Ruiz...Golden lion tamarins are an adaptable species well able to live in degraded and secondary